Abstract
Low temperature (LT) is a key environmental stress affecting the growth, development, yield, and quality of wheat (Triticum aestivum L.). To better understand the genetic basis of cold tolerance in wheat, we conducted a genome-wide association study (GWAS) of low-temperature tolerance at the seedling stage. A total of 543 accessions were genotyped by high-density 90K Illumina iSelect single nucleotide polymorphism (SNP) array, based on phenotypic tests in six environments. We detected 63 loci including 76 significant SNPs associated with cold resistance. These significant SNPs were scattered over 18 chromosomes, which associated with 361 unique candidate genes. Furthermore, by combining transcriptome and GWAS analysis, we additionally identified 85 candidate genes related to cold resistance. These results offer new insights into the genetic basis of cold tolerance, and the linkage markers generated in this study should contribute to molecular-assisted breeding of cold tolerance in wheat.
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Data availability
The sequencing reads of Jing411 were submitted to the NCBI GEO database and are accessible under accession number GSE135474 (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE135474).
References
Båga M, Chodaparambil SV, Limin AE, Pecar M, Fowler DB, Chibbar RN (2007) Identification of quantitative trait loci and associated candidate genes for low-temperature tolerance in cold-hardy winter wheat. Funct Integr Genomics 7(1):53–68. https://doi.org/10.1007/s10142-006-0030-7
Bogdanović J, Mojovic M, Milosavić N, Mitrović A, Vucinić Z, Spasojević I (2008) Role of fructose in the adaptation of plants to cold-induced oxidative stress. Eur Biophys J 37(7):1241–1246. https://doi.org/10.1007/s00249-008-0260-9
Brachi B, Morris GP, Borevitz JO (2011) Genome-wide association studies in plants: the missing heritability is in the field. Genome Biol 12:232. https://doi.org/10.1186/gb-2011-12-10-232
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL, software for association mapping of complex traits in diverse samples. Bioinformatics 23(19):2633–2635. https://doi.org/10.1093/bioinformatics/btm308
Chen XM, He ZH, Wang DS et al (2009) Breeding high-yielding wheat varieties with Jing 411 as backbone parents. Crops 4:1–5
Cushman JC, Bohnert HJ (2000) Genome approaches to plant stress tolerance. Curr Opin Plant Biol 3(2):117–124. https://doi.org/10.1016/S1369-5266(99)00052-7
Dong Y, Liu JD, Zhang Y, Geng H, Rasheed A, Xiao Y, Cao S, Fu L, Yan J, Wen W, Zhang Y, Jing R, Xia X, He Z (2016) Genome-wide association of stem water soluble carbohydrates in bread wheat. PLoS One 11(11):e0164293. https://doi.org/10.1371/journal.pone.0164293
Dunn MA, White AJ, Vural S, Hughes MA (1998) Identification of promoter elements in a low-temperature-responsive gene (blt4.9) from barley (Hordeumvulgare L.). Plant Mol Biol 38(4):551–564. https://doi.org/10.1023/A:1006098132352
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14(8):2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Fowler DB, N'Diaye A, Laudencia-Chingcuanco D, Pozniak CJ (2016) Quantitative trait loci associated with phenological development, low-temperature tolerance, grain quality, and agronomic characters in wheat (Triticum aestivum L.). Plos One 11(3):e0152185. https://doi.org/10.1371/journal.pone.0152185
Gorji AH, Hajianfar R, Rostamforody B (2014) Identification of QTLs associated with cold tolerance in wheat (Triticum aestivum L.). Inter J Agri Biosci 3:45–48
Hou S, Fu D (2014) Methods and influencing factors for cold resistance identification of winter wheat varieties. Beijing Agriculture 3:61–62
Hsu YF, Yu SC, Yang CY, Wang CS (2001) Lily ASR protein-conferred cold and freezing resistance in Arabidopsis. Plant Physiol Biochem 49(9):937–945. https://doi.org/10.1016/j.plaphy.2011.07.002
Jakobsson M, Rosenberg NA (2007) CLUMPP, a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23(14):1801–1806. https://doi.org/10.1093/bioinformatics/btm233
Jeon J, Kim J (2013) Cold stress signaling networks in Arabidopsis. J Plant Biol 56(2):69–76. https://doi.org/10.1007/s12374-013-0903-y
Ju W, Yang C, Zhang S, Tian J, Hai Y, Yang X (2012) Mapping QTL for cell membrane permeability of leaf treated by low temperature in winter wheat. Acta Agron Sin 38:1247–1252
Li H, Peng Z, Yang X et al (2013) Genome-wide association study dissects the genetic architecture of oil biosynthesis in maize kernels. Nat Genet 45(1):43–50. https://doi.org/10.1038/ng.2484
Li Q, Zheng Q, Shen WY, Cram D, Fowler DB, Wei Y, Zou J (2015) Understanding the biochemical basis of temperature-induced lipid pathway adjustments in plants. Plant Cell 27(1):86–103. https://doi.org/10.1105/tpc.114.134338
Li JY, Rasheed A, Guo Q et al (2017) Genome-wide association mapping of starch granule size distribution in common wheat. J Cereal Sci 77:211–218. https://doi.org/10.1016/j.jcs.2017.08.016
Liu K, Muse SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21(9):2128–2129. https://doi.org/10.1093/bioinformatics/bti282
Liu Y, Wang L, Deng M, Li Z, Lu Y, Wang J, Wei Y, Zheng Y (2015) Genome-wide association study of phosphorus-deficiency-tolerance traits in Aegilops tauschii. Theor Appl Genet 128(11):2203–2212. https://doi.org/10.1007/s00122-015-2578-x
Ludwig AA, Romeis T, Jones JD (2004) CDPK-mediated signaling pathways: specificity and cross-talk. J Exp Bot 55(395):181–188. https://doi.org/10.1093/jxb/erh008
Lv Y, Guo ZL, Li XK, Ye HY, Li XH, Xiong LZ (2016) New insights into the genetic basis of natural chilling and cold shock tolerance in rice by genome-wide association analysis. Plant Cell Environ 39:556–570. https://doi.org/10.1111/pce.12635
Mao XZ, Cai T, Olyarchuk JG, Wei LP (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21(19):3787–3793. https://doi.org/10.1093/bioinformatics/bti430
Mao XG, Zhang HY, Tian SJ, Chang XP, Jing RL (2010) TaSnRK2.4, an SNF1-type serine/threonine protein kinase of wheat (Triticum aestivum L.), confers enhanced multistress tolerance in Arabidopsis. J Exp Bot 61(3):683–696. https://doi.org/10.1093/jxb/erp331
Medina J, Bargues M, Terol J, Perez-Alonso M, Salinas J (1999) The Arabidopsis CBF gene family is composed of three genes encoding AP2 domain-containing proteins whose expression is regulated by low temperature but not by abscisic acid or dehydration. Plant Physiol 119:463–469. https://doi.org/10.1104/pp.119.2.463
Miller AK, Galiba G, Dubcovsky J (2006) A cluster of 11 CBF transcription factors is located at the frost tolerance locus Fr-Am2 in Triticum monococcum. Mol Gen Genomics 275(2):193–203. https://doi.org/10.1007/s00438-005-0076-6
Ogbonnaya FC, Rasheed A, Okechukwu EC, Jighly A, Makdis F, Wuletaw T, Hagras A, Uguru MI, Agbo CU (2017) Genome-wide association study for agronomic and physiological traits in spring wheat evaluated in a range of heat prone environments. Theor Appl Genet 130(9):1819–1835. https://doi.org/10.1007/s00122-017-2927-z
Ouellet F, Vazquez-Tello A, Sarhan F (1998) The wheat wcs120 promoter is cold-inducible in both monocotyledonous and dicotyledonous species. FEBS Lett 423(3):324–328. https://doi.org/10.1016/S0014-5793(98)00116-1
Oyiga BC, Sharma RC, Baum M, Ogbonnaya FC, Léon J, Ballvora A (2018) Allelic variations and differential expressions detected at quantitative trait loci for salt stress tolerance in wheat. Plant Cell Environ 41(5):919–935. https://doi.org/10.1111/pce.12898
Pasam RK, Sharma R, Malosettin M et al (2012) Genome-wide association studies for agronomical traits in a world wide spring barley collection. BMC Plant Bio 12(1):16. https://doi.org/10.1186/1471-2229-12-16
Pritchard JK, Stephens MJ, Donnelly PJ (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31(3):279–292. https://doi.org/10.1046/j.1365-313X.2002.01359.x
Shen Z (1995) Crop breeding experiment. Beijing, China
Sukumaran S, Dreisigacker S, Lopes M, Chavez P, Reynolds MP (2015) Genome-wide association study for grain yield and related traits in an elite spring wheat population grown in temperate irrigated environments. Theor Appl Genet 128(2):353–363. https://doi.org/10.1007/s00122-014-2435-3
Sun CW, Zhang FY, Yan XF, Zhang X, Dong Z, Cui D, Chen F (2017) Genome-wide association study for 13 agronomic traits reveals distribution of superior alleles in bread wheat from the yellow and Huai Valley of China. Plant Biotechnol J 15(8):953–969. https://doi.org/10.1111/pbi.12690
Sutka J (1994) Genetic control of frost tolerance in wheat (Triticum aestivum L.). Euphytica 77(3):277–282. https://doi.org/10.1007/BF02262642
Thomashow MF, Gilmour SJ, Stockinger EJ, Jaglo-Ottosen KR, Zarka DG (2001) Role of the Arabidopsis CBF transcriptional activators in cold acclimation. Physiol Plantarum 112(2):171–175. https://doi.org/10.1034/j.1399-3054.2001.1120204.x
Tóth B, Galiba G, Fehér E, Sutka J, Snape JW (2003) Mapping genes affecting flowering time and frost resistance on chromosome 5B of wheat. Theor Appl Genet 107(3):509–514. https://doi.org/10.1007/s00122-003-1275-3
Vágújfalvi A, Galiba G, Dubcovsky J, Cattivelli L (2000) Two loci on wheat chromosome 5A regulate the differential cold-dependent expression of the cor14b gene in frost-tolerant and frost-sensitive genotypes. Mol Gen Genet 263(2):194–200. https://doi.org/10.1007/s004380051160
Vágújfalvi A, Galiba G, Cattivelli L, Dubcovsky J (2003) The cold-regulated transcriptional activator Cbf3 is linked to the frost-tolerance gene Fr-A2 on wheat chromosome 5A. Mol Gen Genomics 269(1):60–67. https://doi.org/10.1007/s00438-003-0806-6
Vágújfalvi A, Aprile A, Miller A, Dubcovsky J, Delugu G, Galiba G, Cattivelli L (2005) The expression of several Cbf genes at the Fr-A2 locus is linked to frost resistance in wheat. Mol Gen Genomics 274(5):506–514. https://doi.org/10.1007/s00438-005-0047-y
Wang GJ, Miao W, Wang JY, Ma DR, Li JQ, Chen WF (2013) Effects of exogenous abscisic acid on antioxidant system in weedy and cultivated rice with different chilling sensitivity under chilling stress. J Agron Crop Sci 199(3):200–208. https://doi.org/10.1111/jac.12004
Wang SC, Wong D, Forrest K et al (2014) Characterization of polyploid wheat genomic diversity using a high-density 90,000 single nucleotide polymorphism array. Plant Biotechnol J 12(6):787–796. https://doi.org/10.1111/pbi.12183
Wang XL, Wu DZ, Yang Q, Zeng J, Jin G, Chen ZH, Zhang G, Dai F (2016a) Identification of mild freezing shock response pathways in barley based on transcriptome profiling. Front Plant Sci 7:106. https://doi.org/10.3389/fpls.2016.00106
Wang D, Liu JL, Li CG, Kang H, Wang Y, Tan X, Liu M, Deng Y, Wang Z, Liu Y, Zhang D, Xiao Y, Wang GL (2016b) Genome-wide association mapping of cold tolerance genes at the seedling stage in rice. Rice 9:61. https://doi.org/10.1186/s12284-016-0133-2
Wrzaczek M, Hirt H (2001) Plant MAP kinase pathways: how many and what for? Biol Cell 93(1–2):81–87. https://doi.org/10.1016/S0248-4900(01)01121-2
Yan SP, Zhang QY, Tang ZC, Su WA, Sun WN (2005) Comparative proteomic analysis provides new insights into chilling stress responses in rice. Mol Cell Proteomics 5(3):484–496. https://doi.org/10.1074/mcp.M500251-MCP200
Yang J, Lee SH, Goddard ME, Visscher PM (2011) GCTA, a tool for genome-wide complex trait analysis. Am J Hum Genet 88(1):76–82. https://doi.org/10.1016/j.ajhg.2010.11.011
Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11:R14. https://doi.org/10.1186/gb-2010-11-2-r14
Zhang Z, Ersoz E, Lai CQ, Todhunter RJ, Tiwari HK, Gore MA, Bradbury PJ, Yu J, Arnett DK, Ordovas JM, Buckler ES (2010) Mixed linear model approach adapted for genome-wide association studies. Nat Genet 42(4):355–360. https://doi.org/10.1038/ng.546
Zhang LH, Liang SB, Cui YZ, Zhang L, Yao HP, Jia XL (2014) Comparison of cold resistance in winter wheat and index selection in the south of huanghuaihai. Chinese Agricultural Science Bulletin 30:77–81
Zhao LN, Liu FX, Xu WY, di C, Zhou S, Xue Y, Yu J, Su Z (2009) Increased expression of OsSPX1 enhances cold/subfreezing tolerance in tobacco and Arabidopsis thaliana. Plant Biotechnol J 7(6):550–561. https://doi.org/10.1111/j.1467-7652.2009.00423.x
Zhao RL, Zhao Y, Yi TF, Xiao YR, Zhang SH, Yang XJ (2019a) Cold resistance identification and variety screening of wheat germplasm resources. Journal of Shandong Agricultural University (Natural Science Edition) 50(1):25–30. https://doi.org/10.3969/j.issn.1000-2324.2019.01.005
Zhao Y, Zhou M, Xu K et al (2019b) Integrated transcriptomics and metabolomics analyses provide insights into cold stress response in wheat. Crop J 7(6):857–866. https://doi.org/10.1016/j.cj.2019.09.002
Zhou M, Zhao Y, Yang X et al (2018) Mapping freezing tolerance quantitative trait loci in bread wheat (Triticum aestivum L.) using a doubled haploid population. Int J Ajric Biol 20:2371–2377. https://doi.org/10.17957/IJAB/15.0763
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This research was funded by the National Key Research and Development Program of China (2017YFD0100600) and the Hebei Basic Key Research Program (17966314D).
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XY and JT conceived the project and formulated the scientific objectives; YX, JL, YZ, RZ, KX, and SZ set up the experimental design and performed the data analysis; YZ and JL wrote the draft manuscript; and YZ and XY revised the paper. All authors discussed the results and read and approved the final manuscript for publication.
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Zhao, Y., Li, J., Zhao, R. et al. Genome-wide association study reveals the genetic basis of cold tolerance in wheat. Mol Breeding 40, 36 (2020). https://doi.org/10.1007/s11032-020-01115-x
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DOI: https://doi.org/10.1007/s11032-020-01115-x